Polymorphism and the Red Queen: the selective maintenance of allelic variation in a deteriorating environment

Abstract

Abstract Although allelic variation is ubiquitous in natural populations, our theoretical models are poor at predicting the existence and properties of these observed polymorphisms. In this study, inspired by Van Valen's Red Queen hypothesis, we modeled the effect of viability selection in a deteriorating environment on the properties of allelic variation in populations subject to recurrent mutation. In Monte Carlo simulations, we found that levels of polymorphism consistently built up over time. We censused the simulated populations after 10,000 generations of mutation and selection, revealing that, compared with models assuming a constant environment, the mean number of alleles was greater, as was the range of allele numbers. These results were qualitatively robust to the addition of genetic drift and to the relaxation of the assumption that the viabilities of phenogenotypes containing a new mutation are independent of each other (i.e. incorporating a model of generalized dominance). The broad range of allele numbers realized in the simulated populations—from monomorphisms to highly polymorphic populations—more closely corresponds to the observed range from numerous surveys of natural populations than previously found in theoretical studies. This match suggests that, contrary to the views of some writers, selection may actively maintain genetic variation in natural populations, particularly if the selective environment is gradually becoming harsher. Our simulations also generated many populations with heterozygote advantage, a mismatch with real data that implies that this selective property must arise extremely rarely in natural populations.